Impaired capacity for familiarity after hippocampal damage

Abstract

Recognition memory is thought to consist of two components: recollection and familiarity. Whereas it is widely agreed that the hippocampus supports recollection (remembering the episode in which an item was learned), there is uncertainty about whether it also supports familiarity (simply knowing that an item was encountered but without remembering the learning episode). We tested a counterintuitive prediction that follows from the idea that the hippocampus selectively supports recollection. Patients with hippocampal lesions should have strong experiences of familiarity as often as controls do; however, unlike controls, these experiences should not be accompanied by recollection. Accordingly, with methods that allow participants to report whether they remember an item as encountered previously or whether they simply know it is familiar, patients should express strong familiarity (in the absence of recollection) more often than controls. We indexed strong familiarity and recollection for previously studied words by obtaining confidence ratings together with Remember-Know judgments. The result was that patients provided fewer high-confidence Know responses than controls rather than more. Furthermore, the number of Know responses made by patients was substantially less than was predicted if recollection were impaired. This was true regardless of whether the prediction was based on the assumption that recollection and familiarity are independent or dependent processes. These results suggest that hippocampal lesions impair both recollection and familiarity. Unlike many previous studies of these constructs, the prediction (and the result) is independent of any particular theoretical model, and it holds even if Remember-Know judgments are not process-pure indicators of recollection and familiarity.

Medial Temporal Lobe Function and Recognition Memory: A Novel Approach to Separating the Contribution of Recollection and Familiarity

“…Yet many of these studies have involved comparisons between strong, recollection-based memory and weaker, familiarity-based memory (Squire et al, 2007; Wixted and Squire, 2011), and recent work suggests that fMRI activity in the hippocampus is best detectable when memory is strong (Song et al, 2011a). Furthermore, when strong, recollection-based memories are compared to strong, familiarity-based memories, the evidence suggests that the hippocampus supports both recollection and familiarity (Song et al, 2011b; Smith et al, 2010; Kirwan et al, 2010; Wais et al, 2010). …”

Memory Retrieval in Mice and Men

“…Whereas many studies report a disproportionate effect of hippocampal damage on recollection and associative memory relative to familiarity (Huppert and Piercy 1978;VarghaKhadem et al 1997;Holdstock et al 2002;Yonelinas et al 2002;Giovanello et al 2003;Mayes et al 2004;Aggleton et al 2005), other reports find that hippocampal damage impacts familiarity and recollection to a similar extent (Manns and Squire 1999;Stark et al 2002;Manns et al 2003;Cipolotti et al 2006;Wais et al 2006;Jeneson et al 2010;Kirwan et al 2010;Song et al 2011). Interestingly, a patient with significant perirhinal damage that spared the hippocampus showed impaired familiarity and preserved recollection (Bowles et al 2007).…”

Neurophysiological evidence for a recollection impairment in amnesia patients that leaves familiarity intact

“…P. Yonelinas et al, 2004). However, some amnesic patients with MTL damage suffer from significant deficits in both recollection and familiarity, leading some to speculate that the MTL operates as a memory system that is equally involved in all forms of episodic memory (Gold et al, 2006; Manns, Hopkins, Reed, Kitchener, & Squire, 2003; Song, Wixted, Hopkins, & Squire, 2011; Squire, Zola-Morgan, & Chen, 1988; Squire & Zola, 1997; Wais, 2008; Wais, Wixted, Hopkins, & Squire, 2006; Wixted & Squire, 2011). …”

“…P. Yonelinas, Kroll, Dobbins, Lazzara, & Knight, 1998; A. P. Yonelinas et al, 2002) and/or familiarity (Song, et al, 2011; Stark & Squire, 2003; Wixted & Squire, 2004), the LPC and FN400 correlates are particularly well suited to addressing this with physiological measures. We predicted that if the patients suffer from a selective deficit in recollection, then they should exhibit a reduced or absent LPC, but a normal FN400.…”